Gorteria – Dutch Botanical Archives 42, 2020: 028 – 035 ISSN (online) 2542-8578

Eleocharis ovata and its alien allies in the

E. L. A. N. Simons1, 2, J. J. Wieringa1, S. Gonggrijp3

Key words Abstract – A revision of Dutch herbarium specimens of series Ovatae shows that two exotic species from North America have also been recorded in the Netherlands since 2011– 2012: Eleocharis obtusa and E. engel- alien species mannii. The number of localities of these species is steadily increasing. The native species, E. ovata, nowadays wetlands only occurs on the Ewijkse Plaat along the River Waal, west of . This population appears to be viable, Eleocharis but it is in a highly dynamic environment close to the river, and might disappear again. The current Red list status Ovatae series ‘Sensitive’ with trend ‘unchanged or increased’ is due to confusion with these two exotic species, and may therefore cryptic species be far too optimistic for this species. Although reported as absent from the Iberian Peninsula, the occurrence of E. Eleocharis obtusa ovata in Spain is reinstated. Eleocharis ovata All three species are quite similar in terms of morphology and ecology, but can be distinguished from each other Eleocharis engelmannii on the basis of the fruits (the width of the persistent stylopodium in relation to the dimensions of the achene), the length of the perianth bristles, the number of stamens and the number of stigmas on the style (2 or 3). Eleocharis ovata seems to be bound to large rivers and occurs in vegetations belonging to the Bidention tripartitae, but is also found on loamy to sandy and rather oligotrophic shores of shallow ponds. The two alien species are found in Bidention tripartitae, Nanocyperion flavescentis or Littorelletea uniflorae vegetations, or transitions between them, but the information on habitats for these two species is limited. For the time being they seem to be bound to slightly poorer soils than E. ovata.

Samenvatting – Na een revisie van het Nederlandse herbariummateriaal van de Eleocharis Ovatae serie blijken twee uit Noord-Amerika afkomstige exotische soorten, die recent gemeld zijn voor België, sinds 2011– 2012 ook aanwezig in Nederland: Eleocharis obtusa en E. engelmannii. Het aantal vindplaatsen van deze soorten neemt gestaag toe. De inheemse soort, E. ovata (Eivormige waterbies), komt nogal onbestendig voor, en is momenteel alleen nog aanwezig op de Ewijkse Plaat, in de Waal ten westen van Nijmegen. Deze populatie lijkt levensvatbaar, maar bevindt zich wel in een hoog dynamisch milieu, en zou dus ook snel weer (bovengronds) kunnen verdwijnen. De huidige status ‘Rode Lijst – Gevoelig’, met trend ‘onveranderd of toegenomen’ komt voort uit verwarring met de twee exoten, en is dan ook veel te optimistisch voor deze soort. In de loop van ons onderzoek stuitten we ook op een collectie van E. ovata uit Spanje. Hiermee hebben we kunnen vaststellen dat de soort, in tegenspraak met moderne literatuur, ook voorkomt op het Iberisch schiereiland. De soorten lijken nogal op elkaar, maar kunnen worden onderscheiden op grond van de vruchten (de breedte van de persistente stijlvoet ten opzichte van de rest van het nootje), de lengte van de perigoonborstels, het aantal meeldraden en het aantal stempels (2 of 3). Eleocharis ovata lijkt vooral gebonden aan grote rivieren en komt daar voor in het Bidention tripartitae, maar is vroeger ook aangetroffen op lemige tot zandige en wat schralere venoevers. De twee uitheemse soorten zijn, voor zover er gegevens op de herbariumcollecties zijn genoteerd, aangetroffen in vegetaties die behoren tot de verbonden Bidention tripartitae, Nanocyperion flavescentis of Littorellion uniflorae.

Published on 14 April 2020

1 Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, corresponding author e-mail: [email protected] the Nether­lands; 2 Simons Botanisch Advies, Leeuweriksweide 229, 6708 LJ Wageningen, the Nether­lands; 3 Pastoor van Kleefstraat 1, 1931 BL, Egmond aan Zee, the Netherlands;

© 2020 Naturalis Biodiversity Center, FLORON & KNBV

You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. Gorteria – Dutch Botanical Archives: 42, 2020 29

INTRODUCTION Deil 2005), are hardly present in the Netherlands. After more than a century and a half, in 2012, the species was found again Eleocharis R. Br. () is a genus comprising about close to the aforementioned locality on the ‘Ewijkse Plaat’, the 250 species (Govaerts et al. 2007), with a more or less world- location of a river wetland restoration project by E. Slootweg. wide distribution, having the largest concentration of species in This population is probably not older than a few decades, as the New World. The Flora of North America reports 67 species local works for nature restoration were carried out in 1989. (Galen Smith et al. 2002), whereas only a small number of Before that year, suitable habitat was probably not available. species is recognized in Europe. Walters (1980) reports 15 Collections of other populations in the Netherlands have been species and Jiménez-Mejías & Luceño (2011) recognize 17, made at three other localities in Middle-Limburg and in the of which 4 introduced. Six taxa have been recorded in the Sliedrechtse Biesbosch (Province of Zuid-Holland) between Netherlands (Reichgelt 1956, van der Meijden 2005). 1994 and 2002. At two out of those three localities, wetland restoration by means of topsoil removal had taken place, result- Eleocharis is characterized by several morphological reduc- ing in ephemeral pioneer communities. Hitherto, in total only 11 tions. The consists of a cluster of unbranched stems, herbarium collections from 4 Dutch localities are known. The each terminating in an inflorescence consisting of a single spike population on the Ewijkse Plaat, estimated to consist of up to (called ‘spikelet’ in almost all literature on this genus). Leaves 40 (waarneming.nl), seems to be the only extant one in are reduced to tubular basal sheaths, which occasionally bears 2018, with no records in 2019. a tiny blade. Despite the overall morphological simplicity, there is significant variation within the genus regarding how this However, from 2011 onwards, some new populations of reduced morphology is shaped and organized. Hence, most Eleocharis ovata were reported from Friesland, eastern Noord- taxa are distinguished based on a limited number of characters. Brabant and northern Limburg, away from the known localities and in different, non-fluviatile habitats. Since Verloove (2015) Infrageneric classification has been complex, with sub­division recorded two closely related species of North American origin into sections or subgenera, sometimes including series of of this series in Belgium (Eleocharis obtusa (Willd.) Schult. and which some are even divided into subseries (Svensson 1929, E. engelmannii Steud.), the identity of those new populations 1932, 1934, 1937, 1939, and later González-Elizondo & in the Netherlands aroused suspicion to us and other Dutch Peterson 1997). Many of those groups turned out to be non- botanists. After examination of herbarium specimens in L and monophyletic (Roalson et al. 2010). No infrageneric taxa have WAG (herbarium acronyms follow Thiers (2019+)) and some been mentioned in the Flora Europaea (Walters 1980), or in field work, the aforementioned North American species turned standard works for the Netherlands (van der Meijden 2005, out to be present in the Netherlands as well. What turned out to Reichgelt 1956). be the first Dutch specimen of E. obtusa was collected by H. J. Eleocharis series Ovatae Svenson (in subgenus Eleocharis, Jager in 2011 near Drachten (Province of Friesland) and a year section Eleogenus (Nees) Benth. & Hook. f.) is a well-supported later, J. H. P. Bruinsma collected the first Dutch specimen of E. clade nested in a badly resolved clade on the (sub)section level engelmannii Steud. at Son (Province of Noord-Brabant). At (Roalson et al. 2010). present, there are four populations for each of these two non- Eleocharis series Ovatae comprises six species, of which five native species (Fig. 1). are resticted to North-America and one can be considered a circumboreal species (Galen Smith et al. 2002). They are wet- land species, generally caespitose annuals with a fibrous root RECOGNITION, DISTRIBUTION AND ECOLOGY OF THE system. However, in North America plants have been observed SPECIES with ascending rhizome-like roots, and it seems likely that such plants survive the winter (Galen Smith et al. 2002). All species Eleocharis ovata (Roth) Roem. & Schult., Systema Vegeta- have brown, smooth, biconvex achenes, with compressed bilium 2, ed. 15 [= ed. 16]: 152. 1817. stylopodia (also called ‘tubercles’), and a base chromosome Basionym: ovatus Roth, Tent. Fl. Germ. 2(2): 562. 1793; number of n = 5. Stylopodium base dimensions and perianth Catal. Bot. 1: 5. 1797. bristle characters are taxonomically the most important and reliable. Stamen and stigma numbers are difficult to observe Scirpus soloniensis Dubois, Meth. Eprouv., ed. 2: 249. 1833. and are often variable within species. Information on style – Eleocharis soloniensis (Dubois) H. Hara, J. Jap. Bot. 14: dimensions or illustrations of styles are absent from modern 338. 1938. treatments. The style is cadu­cous and specimens are usually Eleocharis ovata (Roth) Roem. & Schult. var. heuseri Uechtr., collected and identified with ripe fruits, and hence without styles. Jahresber. Schles. Ges. Vater. Cult. 44: 80. 1866. Anthers are often caducous, and the remaining filaments are often not easily distinguished from the perianth bristles. Therophyte. Caespitose herb, culms ascendant (previously treated Until recently, the only known species of Eleocharis series as var. heuseri Uechtr.) to erect, 5 – 24 cm tall, 0.3 – 0.9 mm wide, Ovatae in the Netherlands was E. ovata (Roth) Roem. & round to subcompressed, shallowly ridged, glabrous, light green. Schult. (Reichgelt 1956, as E. soloniensis (Dubois) H. Hara). It has always been an extremely rare ephemeral species Fibrous roots, rhizomes absent. Leaf sheaths 1– 3, light brown to in the Netherlands, appearing on muddy, loamy or clayey orangish red (at base), distal leaf sheath 0.6 – 3.2 cm, apiculate shores of rivers, former river branches, fens and ponds. to mucronate (rudimentary leaf lamina). The first herbarium specimen of E. ovata dates from 1848, Inflorescence a single spike, ovoid to ovoid-globose 2.5 –10 × collected by T. H. A. J. Abeleven near Weurt, in the Province 1.5 – 4 mm; densely flowered, apex blunt to obtuse. Basal 2 of , on the banks of the River Waal. From the glumes empty; basal most glume subamplexicaul; fertile glumes 1850s onward, however, the large rivers in the Netherlands ovate, c. 1.5 × 0.5 mm, apex acute to obtuse, membranous, were ‘normalized’ (van Heezik 2007), resulting in a drastic abaxially green when young, turning dark brown to blackish reduction of suitable habitats (muddy banks) for this species. brown when ripe, darker than in E. obtusa and E. engelmannii This could explain the rarity of this species ever since, as the (Fernald 1899), adaxially blood-red to purple, margin narrowly bottoms of temporarily drained fishponds, another important hyaline. Perianth bristles 6, c. 1.5 × as long as achene (including habitat for annual wetland species in Europe (Prach et al. 1987, stylopodium), retrorsely spinulose. Stamens 2, anthers c. 0.5 mm. 30 Gorteria – Dutch Botanical Archives: Jaargang 42, 2020

Eleocharis engelmannii Eleocharis obtusa Eleocharis ovata

2018

2011

2018

2012 1999 1848

2018 2012 2017

1998 2011 2016 2018 2002 1994

Fig. 1. Distribution map of the three species belonging to Eleocharis R. Br. series Ovatae Svenson in the Netherlands based on herbarium specimens preserved in the herbarium of Naturalis Biodiversity Center (L and WAG). The localties are labelled with collection year of the specimens. The herbarium specimens were georeferenced and the information was entered into the Naturalis database BRAHMS.

Style 2-branched. No information on style dimensions is known found in eutrophic environments, in vegetations belonging to the from literature, but Fig. 2 shows a bifid style of approximately the Bidention tripartitae, sometimes with Nanocyperion flavescentis same length as an unripe achene (unfortunately, in our herbarium elements. However, a collection from Schinveld/Russcherbeek specimens, no styles were present). Achene biconvex, white (van Moorsel s.n. (L) describes a loamy sandy soil with Juncus when unripe, but turning glossy brown at maturity, obovoid, c. bulbosus L., J. articulatus L., Baldellia ranunculoides (L.) Parl., 0.8 × 0.5 mm, smooth; stylopodium deltoid in side view, when Agrostis stolonifera L., Potamogeton pusillus L. and Alisma ripe c. 1/3 as long and c. 1/2 as wide as achene, dorsiventrally plantago-aquatica L., clearly indicating more meso- or oligo- compressed, apex acuminate. Fl. and fr. July – October. — Fig. 2. trophic conditions. In Central Europe, the species is often found Chromosome number: 2n = 10. in vegetation on fishpond bottoms with a species composition that can be classified as the Eleocharition ovatae (Šumberová Habitat — Pioneer vegetations on sandy, loamy or more often & Lososová 2011). clayish soil of shallow ponds, fens and lakes falling dry (late) in the summer. In the Netherlands, it has predominantly been Gorteria – Dutch Botanical Archives: 42, 2020 31

Fig. 2. Eleocharis ovata (Roth) Roem. & Schult., Ewijkse Plaat (Province of Gelderland), 2012. Left: habit. Right: (unripe) achenes. Photos: Erik Slootweg.

Distribution — More or less circumboreal. Europe, but absent Given that the species is extremely rare (known from just one from Great Britain and Ireland, and Fennoscandia. According locality) and ephemeral in the Netherlands, and declining in to Jiménez-Mejías & Luceño (2011) it is present in Malta and many parts of Europe, the status Critically Endangered would Albania. However, the only record from Malta (Gozo Island) in the make more sense in a next edition of the Dutch Red List. Apart Dutch herbaria we found (K. U. Kramer & L. Y. T. Westra 5352, U from that, there is a possibility that the non-native congeners [U.1239312]), proved to be a very caespitose form of E. palustris could outcompete Eleocharis ovata. (L.) Roem. & Schult., possibly other such collections from Malta have also been mistaken for E. ovata. According to Jiménez Mejías , Synopsis Plantarum Gluma­ & Luceño (2008) the species does not occur in the Iberian Penin- Eleocharis engelmannii Steud. cearum 2: 79. 1855. sula, but we found at least two specimens belonging to E. ovata from Spain: Elias s.n. (U [U.1239311]) from Bugedo in Castilla y León and Merino s.n. (U [U.1239315]) from La Guardi de Ponte­ Eleocharis ovata (Roth) Roem. & Schult. var. engelmannii vedra in Galicia, on the shore of the river that forms the border (Steud.) Britton, J. New York Microscop. Soc. 5: 103. 1889. with Portugal, making it likely it can be found in Portugal as well. Eleocharis obtusa (Willd.) Schult. var. engelmannii (Steud.) Further distribution — Japan, Kazakhstan, Russia (Lunkai & Gilly, Iowa State Coll. J. Sci. 21: 92. 1946. Strong 2010), Canada, USA (Galen Smith et al. 2002). Eleocharis engelmannii Steud. var. detonsa A. Gray ex Patt., Distribution in the Netherlands — Province of Gelderland: First Cat. Pl. Illinois: 46. 1876. record for the Netherlands collected in Weurt, close to Nijmegen Eleocharis engelmannii Steud. f. detonsa (A. Gray ex Patt.) by Abeleven in 1848 (see Appendix). Since 2012, a more or less Svenson, Rhodora 31: 208. 1929. stable population at the ‘Ewijkse Plaat’. Province of Limburg: Russcherbeek, Areven and several collections from the Stevol­ Eleocharis ovata (Roth) Roem. & Schult. var. detonsa (A. Gray plas, close to the River Meuse. Province of Zuid-Holland: A single ex Patt.) Mohlenbr., Ill. Fl. Illinois, Sedges: Cyperus to Scleria, collection from the Biesbosch (Rhine & Meuse estuaries), first ed. 2: 195. 2001. recorded and collected by A. Boesveld in 1999 and probably Eleocharis monticola Fernald, Proc. Amer. Acad. Arts 34: 496, present there until 2009. We doubt the species can quickly re- f. 45 – 50. 1899. appear there. No information on seed longevity of this species is Therophyte. Caespitose herb, culms erect, 10 – 24 cm tall, present in the LEDA plant trait database (Kleyer et al. 2008), but 0.8 – 2.2 mm wide, round to subcompressed, shallowly ridged, the data of other species of Eleocharis that are present, suggest glabrous, light green. Fibrous roots, rhizomes absent. Leaf that the seedbank is transient. sheaths 1 – 3, deep purple red (at base), distal leaf sheath up to Most localities are situated in the Meuse-Rhine river corridor, 4 cm, apiculate to mucronate (rudimentary leaf lamina). connecting the Netherlands, as an ‘outpost’, to the Central- and Inflorescence a single spikelet, ovoid to ovoid-cylindric 4 – 18 × 2 – 4 West-European distribution area. mm; densely flowered, apex bluntly acute to obtuse. Basal 2 glumes According to Sparrius et al. (2014), the Dutch Red List status empty; basal most glume subamplexicaul; fertile glumes ovate, for this species is ‘gevoelig’ (‘Near Threatened’, following IUCN c. 1.5 × 0.5 mm, apex acute to obtuse, membranous, abaxially terminology). At the time the Red List was constructed, the green when young, turning dark brown when ripe, adaxially number of records was overestimated, because the records of blood red-purple, margin narrowly hyaline. Perianth bristles 6, the non-native species Eleocharis obtusa and E. engelmannii c. as long as achene (including stylopodium) or shorter, or ab- had been identified as E. ovata. sent (hence the variation/forma ‘detonsa’), retrorsely spinulose. 32 Gorteria – Dutch Botanical Archives: Jaargang 42, 2020

Stamens (2 – )3, anthers c. 0.5 mm. Style (2 – )3 branched. points towards a common introduction pathway. Scirpus geor- Achene biconvex, white when unripe, but turning glossy brown gianus and Eleocharis engelmannii could have been introduced at maturity, obovoid, c. 1 × 0.8 mm, smooth; stylopodium deltoid in Europe by military troops (Plieninger 2001, Verloove 2015, in side view, when ripe about as wide as achene, c. 0.2 x 0.8 2019). This is most likely the case here, because the locality is mm, dorsiventrally compressed, apex acuminate. Fl. and fr. situated on a former military terrain and there has been a lot of July – December. — Fig. 3. military activity in the Eindhoven area since the Second World Chromosome number: 2n = 10. War. Introduction by military activity might also be the case for the two other localities in the southern part of the Netherlands Habitat — Pioneer vegetations on sandy or loamy soil of shallow where E. engelmannii occurs. However, introduction by military ponds, fens and lakes falling dry (late) in summer. The plants troops is unlikely for the occurrence in Heerhugowaard. Pos- in Heerhugowaard were found in a new residential area, in dis- sible introduction pathways to this locality could have been the turbed soil near a recently excavated ditch. Not much is known transportation of seeds by human-transported soil or dispersal yet on the phytosociological position of this species in the Nether­ of seeds by birds (avichory). lands. The label of Simons & Gonggrijp 2121 (WAG), indicates Lythrum portula (L.) D. A. Webb, setacea, Callitriche Note — The absence, reduction, or caducity of perianth bristles brutia (L.) R. Br., Bolboschoenus laticarpus Marhold, Hroudová, and / or the absence of spines on bristles is supposed to be an Ducháček & Zákr., Scirpus georgianus R. M. Harper, Typha adaption to tidal environments for some Cyperaceae formerly latifolia L., and Carex scoparia Willd. as accompanying species. placed in Scirpus (Schuyler 1972, Strong 1994). This is true for Eleocharis diandra C. Wright and E. aestuum Hines ex A. Haines, Distribution — Canada, USA (Galen Smith et al. 2002). In Europe now recorded from Belgium, The Netherlands, and but E. mutata (L.) Roem. & Schult., often occurring on tidal mud Germany (Plieninger 2001, Verloove 2015), but possibly over- flats has robust and spiny bristles. Eleocharis engelmannii, a looked elsewhere. species that also has more or less reduced perianth bristles, could hardly be considered having a tidal ecology, rendering Distribution in the Netherlands — First record for the Nether- the relation between the habitat and the reduction of bristles lands is a collection made by J. H. P. Bruinsma in 2012 in Son, highly questionable. north of Eindhoven, Province of Noord-Brabant (Bruinsma s.n., L [L.2058156]). The first and the third authors collected the species at or very close to the same location in 2017. They Eleocharis obtusa (Willd.) Schult., Mant. 2: 89. 1824. described the location on the label of the aformentioned col- Basionym: Scirpus obtusus Willd., Enum. Pl. 1: 76. 1809. lection Simons & Gonggrijp 2121 as a former military terrain which has become a suburban village. In 2018, W. Lammers found the species near Halsteren, which is also located in the Therophyte. Caespitose herb, culms ascendant to erect, 10.5 – 24 Province of Noord-Brabant, but more than 100 km west of Son. cm tall, 0.8 – 0.9 mm wide, round to subcompressed, shallowly In 2016, T. O. V. Muusse found the species close to Weert in ridged, glabrous, light green. Fibrous roots, rhizomes absent. the Province of Limburg, c. 50 km southeast of Son. The most Leaf sheaths 1 – 3, deep purple red (at base), distal leaf sheath recent find was made by the third author and the local group 2.5 – 4.0 cm, apiculate to mucronate (rudimentary leaf lamina). of the Dutch Associaton of Field Biology (KNNV Alkmaar-Den Inflorescence a single spikelet, ovoid to ovoid-cylindric 4 – 9 × 2 – 4 Helder) in Heerhugowaard, Province of Noord-Holland, c. 160 mm; densely flowered, apex blunt to obtuse. Basal 2 glumes empty; km northwest of Son. basal most glume subamplexicaul; fertile glumes ovate, c. 1.5 Two of the accompanying species annotated on the label of × 0.5 mm, apex acute to obtuse, membranous, abaxially green Simons & Gonggrijp 2121, Scirpus georgianus and Carex when young, turning dark brown when ripe, adaxially blood red- scoparia, are species native to (Eastern) North America. The purple, margin narrowly hyaline. Perianth bristles 6, c. 1.5 × as presence of three North American species at the locality in Son long as achene (including stylopodium), retrorsely spinulose.

Fig. 3. Eleocharis engelmannii Steud. Left: habit at Son (Province of Noord-Brabant), 2017. Right: (unripe) achenes, Heerhugowaard (Province of Noord- Holland), 2018. Photos: Sipke Gonggrijp. Gorteria – Dutch Botanical Archives: 42, 2020 33

Fig. 4. Eleocharis obtusa. (Willd.) Schult. Left: habit at De Hamert - Nieuwe Heerenven Zuid (Province of Limburg), 25-08-2017. Right: achene at Boukoul (Province of Limburg), 21-08-2013. Photos: Nick van der Ham (left), Sipke Gonggrijp (right).

Stamens (2 – )3, anthers c. 0.5 mm. Style with (2 – )3 branches. (Cyperus fuscus L., Juncus bufonius L. (= J. ranarius Songeon Achene biconvex, white when unripe, but turning glossy brown & E. P. Perrier), Gnaphalium luteo-album L.), Bidention tripartitae at maturity, obovoid, c. 0.8 × 0.5 mm, smooth; stylopodium del- species (Bidens radiata Thuill., B. tripartita L., Persicaria species, toid in side view, when ripe c. 1/3 as long and c. 1/2 as wide as Rumex maritimus L.), and Littorelletea species (Elatine hexandra achene, dorsi­ventrally compressed, apex acuminate. Fig. 4. Fl. (Lapierre) DC., Eleogiton fluitans (L.) Link (≡ Isolepis fluitans (L.) and fr. July – October. — Fig. 4. R. Br.), Baldellia ranunculoides subsp. ranunculoides).’ In Italy, Chromosome number: 2n = 10. the species has become naturalised and grows as a weed in rice fields (Koch 1952, Pignatti 1982). Habitat — Pioneer vegetations on sandy, loamy soil of shallow ponds, fens and lakes falling dry (late) in summer. All localities Distribution — Canada, USA, Hawaii included (Galen Smith et al. are nature restoration projects. At present, not much is known 2002). Europe: Italy (Koch 1952, Walters 1980), Switzerland­ (Des- about the ecology of this species in the Netherlands, but this fayes 2007), Belarus (Dzhus 2014), and Belgium (Verloove 2015). species seems to be more restricted to mesotrophic and oligo- Distribution in the Netherlands — The first record for the Nether­ trophic environment than Eleocharis ovata. The latter species lands was collected by H.J. Jager, who found the species close has been recorded in oligotrophic, mesotrophic, and eutrophic to Drachten (Province of Friesland) in August 2011. Later in this environments. Simons et al. 2083 (WAG) mentions: ‘Muddy shore year it was found in Swalmen (Province of Limburg). So far, the of pond falling dry in (late) summer, on loamy more or less oligo- species has only been found in these two provinces. The locali- trophic soil, rich in sulphate. Together with Nanocyperion species ties in Limburg are in proximity to the Meuse valley, but are not

Table 1. Diagnostic characters of the three Eleocharis species treated in the present study. The symbol # means 'number (of)'.

species stylopodium # stigmas # stamens length of colour of habit perianth bristle basal leaf sheaths shape width width / (in mm) achene width

E. ovata deltoid, 0.3 – 0.5 2 / 3 2 2 greatly exceeding light brown- thin slender stems equilateral in achene length orange side-view (1.5 x)

E. obtusa wider than high 0.5 – 0.9 7 / 10 – 9 / 10 (2 – ) 3 (2 – ) 3 exceeding (wine-)red thick erect stems achene length E. engelmannii much wider 0.5 – 0.9 9 / 10 (2 – ) 3 (2 – ) 3 at most equal- (wine-)red stout plant with thick than high, ling stylopodium erect stems depressed length; some perianths absent 34 Gorteria – Dutch Botanical Archives: Jaargang 42, 2020 situated in the river bed or on river deposits. The localities in REMARKS Friesland are not close to any (large) river system. There are several possible pathways of introduction for new The presence of two alien species of the Eleocharis series populations of Eleocharis obtusa in Europe and the Netherlands. Ovatae from North America raises the question whether other First, around military bases, introduction could have been by species belonging to this North American group (see Fernald unintentional transport of achenes by persons and vehicles. 1899, Galen Smith et al. 2002, Svensson 1929) could emerge This process may be ‘ongoing’. For example, in Belgium, the in Europe as well. They are: species mostly occurs in areas that are, or have been used as, military training areas (Verloove 2015). In the Elsenborn Military — Eleocharis diandra C. Wright occurs in northeastern North American Camp Eleocharis obtusa was accompanied by, among other lakeshores and estuaries. The species resembles E. ovata in having 2 species, the North American Scirpus georgianus (Lambinon stamens, bifid styles, and a depressed stylopodium, which is 1/ 3 – 1/ 2 & Mause 2010), the same species that was found at the E. as long as wide and less than 2 / 3 as wide as the achene. It differs engelmannii locality at Son. from E. ovata by its reduced perianth bristles. — Eleocharis aestuum Hines ex A. Haines resembles E. diandra and A second option is transport of seeds or viable plant parts with has an almost identical distribution, but differs in morphology in hav- plant or soil material for commercial trade. In Belarus, Eleocharis ing no or only 2 – 4 perianth bristles, non-depressed stylopodia, and obtusa was found in cranberry plantations (Dzhus 2014), where stramineous or whitish achenes (Haines 2001). it was found growing together with other (invasive) species — Eleocharis lanceolata Fernald from the southern states in the Missis­ originating from North America. These plantations were planted sippi Basin, Texas, and California, resembles E. engelmannii and E. with cranberry (Vaccinium macrocarpon Aiton) imported from obtusa, but differs from these species in having slender, almost capil- Wisconsin, USA, in the 1980s. It is beyond doubt that E. obtusa lary culms, acuminate-lanceolate spikes, and elongated stylopodia. and the other North American species have unintentionally been intro­duced in these plantations by the import of cranberry planting Of these three species, Eleocharis lanceolata seems to be stock. The population of E. obtusa in Swalmen is close to a V. confined to warmer climates than the North-West European corymbosum farm. Vaccinium corymbosum L. is also native to climate. In their areas of origin, E. diandra and E. aestuum grow North America and it is almost certain that also in this case E. ob- in similar climates as occurring in North-West Europe, but these tusa was introduced by importing North Armerican planting stock. two species are quite rare in North America (Haines 2001). A third option is hydrochory and / or avichory, a more natural way of seed dispersal by water or birds from other European REFERENCES populations. For the Netherlands, this is likely the case for the populations in Limburg, which are situated more or less close to the River Meuse. These populations may originate from Deil U. 2005. A review on habitats, plant traits and vegetation of ephemeral populations of Eleocharis obtusa that occur in the northeastern wetlands-a global perspective. Phytocoenologia 35: 53 –706. Desfayes M. 2008. Flore aquatique et palustre du Valais et du Chablais vaudois: part of Belgium close to the Belgium / Dutch border in Limburg additions. Bull. Murithienne 125: 99 –124. (Verloove 2015). Dzhus MA. 2014. Alien species of American origin on cranberry plantation in Bela­rus (in Russian). Bot. Zhurn. (Moscow & Leningrad [St. Petersburg]) 99: 540 – 554. Drapalik DJ, Mohlenbrock RH. 1960. A Study of Eleocharis, Series Ovatae. KEY TO THE THREE ELEOCHARIS SPECIES Amer. Midl. Naturalist. 64: 339 – 341. Fernald ML. 1899. Eleocharis ovata and its American allies. Contr. Gray Herb., Ser. 2, 15: 485 – 497; Proc. Amer. Acad. Arts. 34: 485 – 497. The key to the three Eleocharis species treated in the present Galen Smith S, Bruhl JJ, Socorro González-Elizondo M, Menapace FJ. 2002. study is based on the keys by Galen Smith et al. (2002), Verloove Eleocharis R. Brown. In: Flora of North America Editorial Committee (ed.), (2015), and the examination of Dutch herbarium specimens. The Flora of North America 23: 60 –120. Oxford University Press,Oxford. diagnostic characters are listed in Table 1. González-Elizondo MS, Peterson PM. 1997. A classification of and key to the supraspecific taxa in Eleocharis (Cyperaceae). Taxon 46: 433 – 449. Govaerts R, Simpson DA, Bruhl JJ, Egorova T, Goetghebeur P, Wilson K. 2007. 1. Stylopodium about as wide as achene, 0.5 – 0.9 mm wide. World checklist of Cyperaceae, Sedges. Kew Publishing, Kew. Basal leaf sheaths red to wine red. Culms erect, 0.8 – 2 mm Haines A. 2001. Eleocharis aestuum (Cyperaceae), a new tidal river shore wide, often robust, 10.5 – 23 cm tall. Stamens predominantly spikesedge of the Eastern United States. Novon 11: 45 – 49. van Heezik AAS. 2007. Strijd om de rivieren; 200 jaar rivierenbeleid in Neder­ 3. Styles predominantly 3-branched ...... 2 land. HNT Historische producties, Rijkswaterstaat, Den Haag / Haarlem. 1. Stylopodium about 2 / 3 as wide as achene or less, 0.3 – 0.5 Jiménez Mejías P, Luceño M. 2008. Eleocharis. In: Castroviejo S, Aedo C, mm wide. Basal leaf sheaths light brown to orange. Culms Laínz M, Muñoz Garmendia F, Nieto Feliner G, Paiva J, Benedí C (eds.), ascendant to erect, up to 0.9 mm wide, often slenderer, Flora iberica 18: 75 – 91. Real Jardín Botánico, CSIC, Madrid. 5 – 24 ( – 35) cm tall. Stamens predominantly 2. Styles Jiménez-Mejías P, Luceño M. 2011. Cyperaceae. In: Euro+Med Plantbase – 2-branched ...... Eleocharis ovata the information resource for Euro-Mediterranean plant diversity. Available at http://ww2.bgbm.org/EuroPlusMed/PTaxonDetail.asp?NameCache=Eleo- charis&PTRefFk=7400000. Accessed 12 December, 2019. 2. Stylopodium 1/ 3 –1/ 2 as long as achene, at least 2 / 3 as long Kleyer M, Bekker RM, Knevel IC, Bakker JP, Thompson K, Sonnenschein M, as wide. Perianth bristles exceeding stylopodium in length Poschlod P, van Groenendael JM, Klimes L, Klimesová J, Klotz S, Rusch GM, Hermy M, Adriaens D, Boedeltje G, Bossuyt B, Dannemann A, Endels ...... Eleocharis obtusa P, Götzenberger L, Hodgson JG, Jackel A-K, Kühn I, Kunzmann D, Ozinga 2. Stylopodium at most 1/ 4 as long as achene, 1/10 – 2 / 5 as long WA, Römermann C, Stadler M, Schlegelmilch J, Steendam HJ, Tackenberg as wide. Perianth bristles at most equally long as stylopodium,­ O, Wilmann B, Cornelissen JHC, Eriksson O, Garnier E, Peco B. 2008. The or (partially) absent ...... Eleocharis engelmannii LEDA Traitbase: A database of life-history traits of Northwest European flora. Journal of Ecology 96: 1266 –1274. Last Update: October 28th, 2008. Leda website and database accessed in October, 2019. Koch W. 1952. Zur Flora der oberitalienischen Reisfelder. Ber. Schweiz. Bot. Ges. 62: 628 – 663. Lambinon J, Mause R . 2010. Deux Eleocharis (Cyperaceae) nouveaux pour la flore belge: E. austriaca et E. obtusa au Camp d’Elsenborn (Haute-Ardenne). Dumortiera 98: 1– 5. Gorteria – Dutch Botanical Archives: 42, 2020 35

Larson BMH, Catling PM. 1996. The separation of Eleocharis obtusa and Eleo- In: Chytrý M (ed.), Vegetace České republiky. 3. Vodní a mokřadní vegetace charis ovata (Cyperaceae) in eastern Canada. Canad. J. Bot. 74: 238 – 242. (Vegetation of the Czech Republic. 3. Aquatic and Wetland Vegetation): Lunkai D, Strong MT. 2010. Eleocharis R. Br. In: Flora of China. Missouri Bo- 347– 381. Academia, Praha. tanical Garden, St. Louis, MO & Harvard University Herbaria, Cambridge, Svenson HK. 1929. Monographic studies in the genus Eleocharis. I. Rhodora MA. eFlora version of Eleocharis in Flora of China accessed via the website 31: 121–135, 152 –163, 167–191, 199 – 219, 224 – 242. efloras.org on January, 2019. Svenson HK. 1932. Monographic studies in the genus Eleocharis. II. Rhodora Pignatti S. 1982. Eleocharis. In: Flora d’Italia 3. Edagricole, Bologna. 34: 193 – 203, 215 – 227. Plieninger W. 2001. Ein Fund von Eleocharis engelmannii Steudel bei Heil- Svenson HK. 1934. Monographic studies in the genus Eleocharis. III. Rhodora bronn. Ber. Bot. Arbeitsgem. Südwestdeutschl. 1: 47– -52. 36: 377– 389. Prach K, Květ J, Ostrý I. 1987. Ecological analysis of the vegetation in a Svenson HK. 1937. Monographic studies in the genus Eleocharis. IV. Rhodora summer-drained fishpond. Folia Geobot. Phytotax. 22: 4 –70 39: 210 – 231, 236 – 273. Reichgelt ThJ. 1956. Eleocharis. In: Cyperaceae excl. Carex. Flora Neerlandica Svenson HK. 1939. Monographic studies in the genus Eleocharis. V. Rhodora 1(4): 32 – 40. 41: 1–19, 43 – 47, 90 –110. Roalson EH, Hinchliff CE, Trevisan R, da Silva CRM. 2010. Phylogenetic Thiers B. 2019+ (continuously updated). Index Herbariorum: A global directory Relationships in Eleocharis (Cyperaceae): C 4 Photosynthesis Origins and of public herbaria and associated staff. New York Botanical Garden’s Virtual Patterns of Diversification in the Spikerushes. Syst. Bot. 35: 257– 271. Herbarium, New York. Accessed in January, 2019. Schuyler AE. 1972. Chromosome numbers of Scirpus purshianus and S. Verloove F. 2015. Eleocharis engelmannii and E. obtusa (Cyperaceae), two smithii. Rhodora 74 (799): 398 – 406. recent acquisitions from series Ovatae in Belgium. Dumortiera 107: 25 – 30. Sparrius LB, Odé B, Beringen R. 2014. Basisrapport Rode Lijst Vaatplant- Verloove F. 2019. Scirpus atrovirens. In: Manual of the Alien Plants of Bel- en 2012 volgens Nederlandse en IUCN-criteria. FLORON Rapport 57. gium. Botanic Garden Meise, Belgium. Website at alienplantsbelgium.be, FLORON, Nijmegen. accessed 15 January 2019. Strong MT. 1994. of Scirpus, Trichophorum, and Schoenoplectus van der Meijden R. 2005. Heukels’ Flora van Nederland, ed. 23. Wolters- (Cyperaceae) in Virginia. Bartonia 58: 29 – 68. Noordhoff, Groningen / Houten. Šumberová K, Lososová Z. 2011. Vegetace jednoletých nitrofilních vlhkomil- Walters SM. 1980. Eleocharis R. Br. In: Tutin TG et al. (eds.), Flora Europaea ných bylin (Vegetation of annual nitrophilous wetland herbs, in Czech). 5: 281– 284. Cambridge University Press, Cambridge.

Eleocharis engelmannii — J. H.­P. Bruinsma s.n. (L), 4-12-2012. Son, water­ Appendix berging Sonniuspark. 51°31.91’ N, 5°28.74’ E; E. L. A. N. Simons 2121 (WAG), 4-11-2017. Son, Sonniuspark. 51°31.91’ N, 5°28.74’ E; T. O. V. Muusse s.n. (WAG), 3-9-2016. SW of Weert, Weert - Kettingdijk. 51°12.45’ Herbarium specimens examined N, 5°37.54’ E; W. Lammers s.n. (L, WAG), 2-7-2018. Halsteren - Het Laag. 51°32.43’ N, 4°18.27’ E; S. Gonggrijp 226 (L), 28-8-2018. Heerhugowaard. 52°40.08’ N, 4°48.46. The herbarium specimens that were examined for this study are listed below. Eleocharis obtusa — E. J. Weeda s.n. (L), 20-9-2011. Swalmen, Blankwater. Herbarium acronyms are according to Thiers (2019+). The 51°12.66’ N, 6°03.78’ E; H. J. Jager s.n. (L), 31-8-2011. Azeven. 53°06.5’ abbre­viation ‛s.n.’ stands for ‛sine numero’, i.e. specimens N, 6°08.1’ E; E. L. A. N. Simons 2083 (WAG), 18-8-2017. East of Wellerlooi, without a collection number. Hamert, Nieuwe Heerenven. 51°31.77’ N, 6°11.02’ E; J. Huizenga s.n. (L, WAG), 18-6-2018. Twijzeler­mieden, between Buitenpost and Twijzel. 53°14.32’ N, 6°07.53’ E; N. Eimers s.n. (L), 27-8-2018. Asenray - Elmpter­ Eleocharis ovata — R. C.­M.J.­ van Moorsel s.n. (L), 10-9-1994. Ruscherbeek. broek 51°12.14’ N, 6°04.08’ E. 50°58.8’ N, 5°59.8’ E; E. L. A. N. Simons 921 (WAG), 19-7-2012. East of Ewijk. 51°52.62’ N, 5°46.08’ E Alt: 12m; R. Barendse s.n. (L), 0-8-1998. Het Areven, bij Stamproy. 51°11.70’ N, 5°41.44’ E; A. Boesveld s.n. (L), 30-9- 1999. Sliedrechtse Biesbosch. 51°48.69’ N, 4°51.07’ E; R. Barendse 1630 (L), aug-1998. Het Areven bij Stamproy. 51°11.70’ N, 5°41.44’ E; T. H. A. J. Abeleven 1116 (L), 0-10-1848. Waaloever te Weurt bij Nijmegen. 51°52’ N, 5°49’ E; J. Klinckenberg s.n. (L), 19-8-2002. Stevensweert: Maasplas. 51°07.29’ N, 5°50.62’ E; E. L. A. N. Simons 2101 (WAG), 14-10-2017. Ewijkse Plaat, close to . 51°52.64’ N, 5°46.06’ E; E. J. Slootweg s.n. (L), 19-7-2012. Beuningen, uiterwaarden. 51°52.65’ N, 5°46.07’ E; G. M. Dirkse 8548 (L), 27-7-2012. Beuningse uiterwaarden. 51°52.65’ N, 5°46.07’ E; E. J. Weeda s.n. (L), 5-9-2002. Midden-Limburg, Stevensweert, bij Molenveld. 51°07.3’ N, 5°50.6’ E.